Nrf2-dependent upregulation of antioxidative enzymes: A novel pathway for hypoxic preconditioning-mediated delayed cardioprotection

Molecular and Cellular Biochemistry

Volumn 385, Issue 1-2, 2014, Pages 33-41

  Huang, Xiao Shan ^a   Chen, He Ping ^a   Yu, Hai Hong ^a   Yan, Yu Feng ^a   Liao, Zhang Ping ^a   Huang, Qi Ren ^a  

^a NANCHANG UNIVERSITY   (China)

Author keywords

Delayed cardioprotection; Hypoxia reoxygenation; Hypoxic preconditioning; Nrf2 ARE pathway; Oxidative stress

Indexed keywords

ANTIOXIDANT; HEME OXYGENASE 1; LACTATE DEHYDROGENASE; MANGANESE SUPEROXIDE DISMUTASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONTROLLED STUDY; ENZYME INDUCTION; HEART INFARCTION PREVENTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; ISCHEMIC PRECONDITIONING; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

RATTUS;

ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; ANTIOXIDANTS; CARDIOTONIC AGENTS; CELL HYPOXIA; CELL LINE; CELL NUCLEUS; GENE KNOCKDOWN TECHNIQUES; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCYTES, CARDIAC; NF-E2-RELATED FACTOR 2; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84890554973     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1812-6     Document Type: Article

References (31)

1. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136
2. Arstall MA, Zhao YZ, Hornberger L, Kennedy SP, Buchholz RA, Osathanondh R, Kelly RA (1998) Human ventricular myocytes in vitro exhibit both early and delayed preconditioning responses to simulated ischemia. J Mol Cell Cardiol 30:1019-1025. doi: 10.1006/jmcc.1998.0666
3. Webster KA, Discher DJ, Bishopric NH (1995) Cardioprotection in an in vitro model of hypoxic preconditioning. J Mol Cell Cardiol 27:453-458
4. Yamashita N, Nishida M, Hoshida S, Kuzuya T, Hori M, Taniguchi N, Kamada T, Tada M (1994) Induction of manganese superoxide dismutase in rat cardiac myocytes increases tolerance to hypoxia 24 hours after preconditioning. J Clin Invest 94:2193-2199. doi: 10.1172/JCI117580
5. Yellon DM, Downey JM (2003) Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83:1113-1151. doi: 10.1152/physrev.00009.2003
6. Das DK, Maulik N (2006) Cardiac genomic response following preconditioning stimulus. Cardiovasc Res 70:254-263. doi: 10.1016/j.cardiores. 2006.02.023
7. Bolli R (1996) The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview. Basic Res Cardiol 91:57-63
8. Rizvi A, Tang XL, Qiu Y, Xuan YT, Takano H, Jadoon AK, Bolli R (1999) Increased protein synthesis is necessary for the development of late preconditioning against myocardial stunning. Am J Physiol 277:874-884
9. Vanden Hoek T, Becker LB, Shao ZH, Li CQ, Schumacker PT (2000) Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion. Circ Res 86:541-548
10. Morihira M, Hasebe N, Baljinnyam E, Sumitomo K, Matsusaka T, Izawa K, Fujino T, Fukuzawa J, Kikuchi K (2006) Ischemic preconditioning enhances scavenging activity of reactive oxygen species and diminishes transmural difference of infarct size. Am J Physiol Heart Circ Physiol 290:577-583. doi: 10.1152/ajpheart.00817.2004
11. Hoshida S, Yamashita N, Otsu K, Hori M (2002) The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines. Cardiovasc Res 55:495-505
12. Zhou X, Zhai X, Ashraf M (1996) Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocytes. Circulation 93:1177-1184
13. Jancso G, Cserepes B, Gasz B, Benko L, Borsiczky B, Ferenc A, Kurthy M, Racz B, Lantos J, Gal J, Arato E, Sinayc L, Weber G, Roth E (2007) Expression and protective role of heme oxygenase-1 in delayed myocardial preconditioning. Ann N Y Acad Sci 1095:251-261. doi: 10.1196/annals.1397.029
14. Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47:1304-1309. doi: 10.1016/j. freeradbiomed.2009.07.035
15. Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284:13291-13295. doi: 10.1074/jbc.R900010200
16. Sun Z, Zhang S, Chan JY, Zhang DD (2007) Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol 27:6334-6349. doi: 10.1128/MCB.00630-07
17. Howden R (2013) Nrf2 and cardiovascular defense. Oxid Med Cell Longev 2013:104308. doi: 10.1155/2013/104308
18. Lee JM, Johnson JA (2004) An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37:139-143
19. Zhang X, Xiao Z, Yao J, Zhao G, Fa X, Niu J (2013) Participation of protein kinase C in the activation of Nrf2 signaling by ischemic preconditioning in the isolated rabbit heart. Mol Cell Biochem 372:169-179. doi: 10.1007/s11010-012-1458-9
20. Mizukami Y, Iwamatsu A, Aki T, Kimura M, Nakamura K, Nao T, Okusa T, Matsuzaki M, Yoshida K, Kobayashi S (2004) ERK1/2 regulates intracellular ATP levels through alpha-enolase expression in cardiomyocytes exposed to ischemic hypoxia and reoxygenation. J Biol Chem 279:50120-50131. doi: 10.1074/jbc.M402299200
21. Jiao JD, Garg V, Yang B, Hu K (2008) Novel functional role of heat shock protein 90 in ATP-sensitive K+ channel-mediated hypoxic preconditioning. Cardiovasc Res 77:126-133. doi: 10.1093/cvr/cvm028
22. Kim JY, Cho HJ, Sir JJ, Kim BK, Hur J, Youn SW, Yang HM, Jun SI, Park KW, Hwang SJ, Kwon YW, Lee HY, Kang HJ, Oh BH, Park YB, Kim HS (2009) Sulfasalazine induces haem oxygenase-1 via ROS-dependent Nrf2 signalling, leading to control of neointimal hyperplasia. Cardiovasc Res 82:550-560. doi: 10.1093/cvr/cvp072
23. Li J, Ichikawa T, Jin Y, Hofseth LJ, Nagarkatti P, Nagarkatti M, Windust A, Cui T (2010) An essential role of Nrf2 in American ginseng-mediated anti-oxidative actions in cardiomyocytes. J Ethnopharmacol 130:222-230. doi: 10.1016/j.jep.2010.03.040
24. Saeed SA, Waqar MA, Zubairi AJ, Bhurgri H, Khan A, Gowani SA, Waqar SN, Choudhary MI, Jalil S, Zaidi AH, Ara I (2005) Myocardial ischaemia and reperfusion injury: reactive oxygen species and the role of neutrophil. J Coll Physicians Surg Pak 15:507-514. doi: 08.2005/JCPSP.507514
25. Zweier JL, Talukder MA (2006) The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 70:181-190. doi: 10.1016/j.cardiores.2006.02. 025
26. Park JL, Lucchesi BR (1999) Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 68:1905-1912
27. Dhalla NS, Elmoselhi AB, Hata T, Makino N (2000) Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res 47:446-456
28. Rui T, Cepinskas G, Feng Q, Kvietys PR (2003) Delayed preconditioning in cardiac myocytes with respect to development of a proinflammatory phenotype: role of SOD and NOS. Cardiovasc Res 59:901-911
29. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, Kensler TW, Talalay P (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci USA 101:2040-2045. doi: 10.1073/pnas.0307301101
30. Huang HC, Nguyen T, Pickett CB (2002) Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 277:42769-42774. doi: 10.1074/jbc.M206911200
31. Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36:1199-1207. doi: 10.1016/j. freeradbiomed.2004.02.074